Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis

Emilie A. Rennie, Berit Ebert, Godfrey P. Miles, Rebecca E. Cahoon, Katy M. Christiansen, Solomon Stonebloom, Hoda Khatab, David Twell, Christopher J. Petzold, Paul D. Adams, Paul Dupree, Joshua L. Heazlewood, Edgar B Cahoon, Henrik Vibe Scheller

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

Glycosyl inositol phosphorylceramide (GIPC) sphingolipids are a major class of lipids in fungi, protozoans, and plants. GIPCs are abundant in the plasma membrane in plants, comprising around a quarter of the total lipids in these membranes. Plant GIPCs contain unique glycan decorations that include a conserved glucuronic acid (GlcA) residue and various additional sugars; however, no proteins responsible for glycosylating GIPCs have been identified to date. Here, we show that the Arabidopsis thaliana protein INOSITOL PHOSPHORYLCERAMIDE GLUCURONOSYLTRANSFERASE1 (IPUT1) transfers GlcA from UDP-GlcA to GIPCs. To demonstrate IPUT1 activity, we introduced the IPUT1 gene together with genes for a UDP-glucose dehydrogenase from Arabidopsis and a human UDP-GlcA transporter into a yeast mutant deficient in the endogenous inositol phosphorylceramide (IPC) mannosyltransferase. In this engineered yeast strain, IPUT1 transferred GlcA to IPC. Overexpression or silencing of IPUT1 in Nicotiana benthamiana resulted in an increase or a decrease, respectively, in IPC glucuronosyltransferase activity in vitro. Plants in which IPUT1 was silenced accumulated IPC, the immediate precursor, as well as ceramides and glucosylceramides. Plants overexpressing IPUT1 showed an increased content of GIPCs. Mutations in IPUT1 are not transmitted through pollen, indicating that these sphingolipids are essential in plants.

Original languageEnglish (US)
Pages (from-to)3314-3325
Number of pages12
JournalPlant Cell
Volume26
Issue number8
DOIs
StatePublished - Aug 1 2014

Fingerprint

Glucuronosyltransferase
sphingolipids
Sphingolipids
Inositol
Pollen
Arabidopsis
pollen
glucuronic acid
Glucuronic Acid
Uridine Diphosphate Glucuronic Acid
inositols
Uridine Diphosphate Glucose Dehydrogenase
Mannosyltransferases
Yeasts
Arabidopsis Proteins
Glucosylceramides
yeasts
ceramides
Nicotiana benthamiana
Ceramides

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology

Cite this

Rennie, E. A., Ebert, B., Miles, G. P., Cahoon, R. E., Christiansen, K. M., Stonebloom, S., ... Scheller, H. V. (2014). Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis. Plant Cell, 26(8), 3314-3325. https://doi.org/10.1105/tpc.114.129171

Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis. / Rennie, Emilie A.; Ebert, Berit; Miles, Godfrey P.; Cahoon, Rebecca E.; Christiansen, Katy M.; Stonebloom, Solomon; Khatab, Hoda; Twell, David; Petzold, Christopher J.; Adams, Paul D.; Dupree, Paul; Heazlewood, Joshua L.; Cahoon, Edgar B; Scheller, Henrik Vibe.

In: Plant Cell, Vol. 26, No. 8, 01.08.2014, p. 3314-3325.

Research output: Contribution to journalArticle

Rennie, EA, Ebert, B, Miles, GP, Cahoon, RE, Christiansen, KM, Stonebloom, S, Khatab, H, Twell, D, Petzold, CJ, Adams, PD, Dupree, P, Heazlewood, JL, Cahoon, EB & Scheller, HV 2014, 'Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis', Plant Cell, vol. 26, no. 8, pp. 3314-3325. https://doi.org/10.1105/tpc.114.129171
Rennie EA, Ebert B, Miles GP, Cahoon RE, Christiansen KM, Stonebloom S et al. Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis. Plant Cell. 2014 Aug 1;26(8):3314-3325. https://doi.org/10.1105/tpc.114.129171
Rennie, Emilie A. ; Ebert, Berit ; Miles, Godfrey P. ; Cahoon, Rebecca E. ; Christiansen, Katy M. ; Stonebloom, Solomon ; Khatab, Hoda ; Twell, David ; Petzold, Christopher J. ; Adams, Paul D. ; Dupree, Paul ; Heazlewood, Joshua L. ; Cahoon, Edgar B ; Scheller, Henrik Vibe. / Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis. In: Plant Cell. 2014 ; Vol. 26, No. 8. pp. 3314-3325.
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